tools and conceptual frameworks, if we are tounderstand the consequences of resource hetero-geneity and microbial behavior on diversity, pro-ductivity, and biogeochemistry.Roman StockerMarine bacteria influence Earth’s environmental dynamics in fundamental ways by controllingthe biogeochemistry and productivity of the oceans. These large-scale consequences result fromthe combined effect of countless interactions occurring at the level of the individual cells. Atthese small scales, the ocean is surprisingly heterogeneous, and microbes experience anenvironment of pervasive and dynamic chemical and physical gradients. Many species activelyexploit this heterogeneity, while others rely on gradient-independent adaptations. This is anexciting time to explore this frontier of oceanography, but understanding microbial behaviorand competition in the context of the water column’s microarchitecture calls for new ecologicalframeworks, such as a microbial optimal foraging theory, to determine the relevant trade-offsand global consequences of microbial life in a sea of gradients.

Twenty years ago much of microbial ocean- ography was based on the assumption that molecules and organisms are randomly
distributed, with little regard for gradients and
behavioral responses (1). There is now abundant
evidence that nutrients are not homogeneously
distributed at the scales relevant to the microorganisms and instead frequently arise as microscale
hot spots. Many bacteria exploit heterogeneity
by swimming toward the epicenter of hot spots,
whereas others survive in low-concentration, uniform background conditions.

Although tools to interrogate the behavior of
marine microbes at the level of single cells and
their microenvironment have begun to be developed, the conceptual frameworks needed to evaluate the trade-offs and ecosystem implications of
life in microscale gradients lag behind. Integrating microscale observations with ecological frameworks will shed light on important unexplored
questions in microbial oceanography. What are
the effects of gradients on microbial diversity
in the ocean? How do they affect productivity? Do
the consequences of heterogeneity simply average out, justifying mean-field descriptions based
on bulk concentrations and a neglect of behavior,
or do microscale gradients affect the rates and
fluxes of biogeochemical transformation? This
Review describes the nature and prevalence of
microscale gradients in the ocean, the response
of microbes to these gradients, and the putative
mechanisms by which these processes can affect
the marine ecosystem at a global scale.

scale processes in the sea, including the cycling
of most elements, the rates and fate of primary
production, and the generation of climatically
active gases (2), yet they live and interact with the
ocean at the microscale. In terms of relative scale,
environmental conditions at tens of meters resolution are to a microbe what the mean world
temperature is to an African lion: a useful metric
for global trends, but hardly a mechanistic ecological predictor.

How large, then, is a microbial microenvironment in the ocean? Rather than being a fixed
volume (3), it depends on behavior and time, as
simple calculations exemplify. For a nonmotile
bacterium (or archaeon), cell size (~0.4- to 2-mm
diameter) defines the microenvironment. For example, nutrient uptake occurs from a small region
surrounding the organism, the diffusion boundary layer, which spans a few cell diameters. There
is little motion of the cell relative to the surrounding water, with Brownian diffusion allowing a 0.4-mm–diameter cell to explore 45 pl of
seawater (a ~35-mm cube) in 10 min and 80 nl
(a ~430-mm cube) in a day.

In contrast, the microenvironment of a swimming bacterium is largely defined by its motility
range. One can calculate that randomly swimming at 50 mm/s enables a bacterium to experience 0.5 ml (a 0.8-mm cube) of new water every
10 min and 0.8 ml (a ~1 cm cube) every day.
Chemotaxis (the ability to sense chemical gradients and direct motility accordingly) further increases the distance a microbe can traverse: a
chemotactic velocity (the directional component
of swimming) of 10 mm/s results in a net displacement of 6 mm in 10 min.

Microbial microenvironments can thus be large
compared with cell size but are still tiny relative
to most oceanographic sampling methods. With
rare exceptions, these volumes remain difficult
to interrogate in situ, owing to the small size and
intermittency of microenvironments and the minuscule amount of matter they contain. We must gain
better access to the marine microscale, in terms of

How Heterogeneous Is the Oceanat the Microscale?

It has long been recognized that the water column
is dotted with copious sources of microscale heterogeneity (Fig. 1). A ubiquitous case is the “
phycosphere,” the region surrounding a phytoplankton
cell, which harbors gradients of dissolved organic
matter [DOM; operationally defined as the organic material <0.7 mm in size (2)] and oxygen
that attract heterotrophic bacteria (4, 5). This
attraction can result in diverse ecological interactions between bacteria and algae, from symbiosis to parasitism, and can increase the fraction
of primary production used by bacteria (6). Equally widespread are marine snow particles, aggregates that also contain gradients of DOM and
oxygen (7) and emanate intense DOM plumes as
they sink (8, 9). The particles and their plumes
can attract and become growth hot spots for bacteria (9, 10). Strong gradients are further created
by excretions from larger organisms, cell lysis, and
sloppy feeding. These sources of heterogeneity,
along with a multitude of particle types ranging
from colloids to fecal pellets to exopolymers, can
vary in size from micrometers to centimeters, and
harbor resource concentrations orders of magnitude above background levels.

These processes have led to the view that
even a milliliter of seawater is far from homogeneous (3). I suggest that microscale gradients are
in fact considerably more pervasive than even
these sources of heterogeneity indicate, for three
reasons. First, the majority of inputs of microbial
resources are heterogeneous at microbial scales:
10- to 1000-mm oil droplets originating from spills
or natural seeps, 50- to 5000-mm gas bubbles
released from natural vents or injected by breaking
waves, sediment grains resuspended by currents,
and dust particles of aeolian origin are all constituents of large-scale events that for marine
microorganisms resolve into a patchy landscape
peppered with discrete resources and microscale
gradients.

Second, turbulence converts macroheteroge-neity into microheterogeneity. In the process of
mixing a solute such as DOM, turbulent whirls
stir the solute into ever-finer sheets and filaments
(see Box 1 and associated figure). This stretching and folding continues down to a scale below
which molecular diffusion dissipates gradients to
truly mix the solute. For typical marine turbulence
levels, this scale, known as the Batchelor scale,
ranges from 30 to 300 mm. Thus, irrespective of
the size of the DOM source, turbulence produces
a rich fabric of gradients at the scale of microbial
microenvironments.